Reactive oxygen and nitrogen species: multifaceted regulators of ovarian activity†
Language English Country United States Media print
Document type Journal Article, Review
Grant support
QK22010270
Ministry of Agriculture of the Czech Republic
APVV-19-0111
Slovak Research and Development Agency, Slovak Republic
PubMed
39936599
PubMed Central
PMC12078082
DOI
10.1093/biolre/ioaf032
PII: 8010273
Knihovny.cz E-resources
- Keywords
- corpus luteum, nitric oxide, ovarian regulation, oxidative stress, reactive nitrogen species, reactive oxygen species,
- MeSH
- Humans MeSH
- Ovary * physiology metabolism MeSH
- Ovulation physiology MeSH
- Oxidative Stress physiology MeSH
- Reactive Nitrogen Species * metabolism MeSH
- Reactive Oxygen Species * metabolism MeSH
- Signal Transduction MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
- Names of Substances
- Reactive Nitrogen Species * MeSH
- Reactive Oxygen Species * MeSH
Reactive oxygen and nitrogen species are essential components of diverse intracellular signaling pathways. In addition to their involvement in apoptosis, reactive oxygen and nitrogen species are crucial in the regulation of multiple developmental and physiological processes. This review aims to summarize their role in the regulation of key ovarian stages: ovulation, maturation and postovulatory ageing of the oocyte, and the formation and regression of the corpus luteum. At the cellular level, a mild increase in reactive oxygen and nitrogen species is associated with the initiation of a number of regulatory mechanisms, which might be suppressed by increased activity of the antioxidant system. Moreover, a mild increase in reactive oxygen and nitrogen species has been linked to the control of mitochondrial biogenesis and abundance in response to increased cellular energy demands. Thus, reactive oxygen and nitrogen species should also be perceived in terms of their positive role in cellular signaling. On the other hand, an uncontrolled increase in reactive oxygen species production or strong down-regulation of the antioxidant system results in oxidative stress and damage of cellular components associated with ovarian pathologies and ageing. Similarly, the disturbance of signaling functions of reactive nitrogen species caused by dysregulation of nitric oxide production by nitric oxide synthases in ovarian tissues interferes with the proper regulation of physiological processes in the ovary.
Department of Biochemistry Faculty of Science Palacký University Olomouc Czech Republic
Department of Zoology Faculty of Science Palacký University Olomouc Czech Republic
See more in PubMed
Li L, Shi X, Shi Y, Wang Z. The Signaling pathways involved in ovarian follicle development. Front Physiol 2021; 12:730196. PubMed PMC
Thatcher WW. A 100-year review: historical development of female reproductive physiology in dairy cattle. J Dairy Sci 2017; 100:10272–10291. PubMed
Davis JS, Rueda BR. The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci 2002; 7:d1949–d1978. PubMed
Mlyczynska E, Kiezun M, Kurowska P, Dawid M, Pich K, Respekta N, Daudon M, Rytelewska E, Dobrzyn K, Kaminska B, Kaminski T, Smolinska N, et al. New aspects of corpus luteum regulation in physiological and pathological conditions: involvement of adipokines and neuropeptides. Cells 2022; 11:957. PubMed PMC
Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 2012; 10:49. PubMed PMC
Ciani F, Cocchia N, d’Angelo D, Tafuri S. In: Wu B (ed.), Influence of ROS on Ovarian Functions. IntechOpen; 2015: 10.5772/61003. DOI
Fujii J, Iuchi Y, Okada F. Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod Biol Endocrinol 2005; 3:43. PubMed PMC
Basini G, Grasselli F. Nitric oxide in follicle development and oocyte competence. Reproduction 2015; 150:R1–R9. PubMed
Hattori M, Sakamoto K, Fujihara N, Kojima I. Nitric oxide: a modulator for the epidermal growth factor receptor expression in developing ovarian granulosa cells. Am J Phys 1996; 270:C812–C818. PubMed
Luo Y, Zhu Y, Basang W, Wang X, Li C, Zhou X. Roles of nitric oxide in the regulation of reproduction: a review. Front Endocrinol (Lausanne) 2021; 12:752410. PubMed PMC
Nath P, Maitra S. Physiological relevance of nitric oxide in ovarian functions: an overview. Gen Comp Endocrinol 2019; 279:35–44. PubMed
Nishikimi A, Matsukawa T, Hoshino K, Ikeda S, Kira Y, Sato EF, Inoue M, Yamada M. Localization of nitric oxide synthase activity in unfertilised oocytes and fertilised embryos during preimplantation development in mice. Reproduction 2001; 122:957–963. PubMed
Rosselli M, Keller PJ, Dubey RK. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum Reprod Update 1998; 4:3–24. PubMed
Zhao Y, Vanhoutte PM, Leung SW. Vascular nitric oxide: beyond eNOS. J Pharmacol Sci 2015a; 129:83–94. PubMed
Jîtcă G, Ősz BE, Tero-Vescan A, Miklos AP, Rusz CM, Bătrînu MG, Vari CE. Positive aspects of oxidative stress at different levels of the human body: a review. Antioxidants (Basel) 2022; 11:572. PubMed PMC
Kawagishi H, Finkel T. Unraveling the truth about antioxidants: ROS and disease: finding the right balance. Nat Med 2014; 20:711–713. PubMed
Poljsak B, Suput D, Milisav I. Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative Med Cell Longev 2013; 2013:956792. PubMed PMC
Checa J, Aran JM. Reactive oxygen species: drivers of physiological and pathological processes. J Inflamm Res 2020; 13:1057–1073. PubMed PMC
Harris IS, DeNicola GM. The complex interplay between antioxidants and ROS in cancer. Trends Cell Biol 2020; 30:440–451. PubMed
Tang Z, Chen J, Zhang Z, Bi J, Xu R, Lin Q, Wang Z. HIF-1alpha activation promotes Luteolysis by enhancing ROS levels in the corpus luteum of Pseudopregnant rats. Oxidative Med Cell Longev 2021; 2021:1764929. PubMed PMC
Zamberlam G, Sahmi F, Price CA. Nitric oxide synthase activity is critical for the preovulatory epidermal growth factor-like cascade induced by luteinising hormone in bovine granulosa cells. Free Radic Biol Med 2014; 74:237–244. PubMed
Motta AB, Estevez A, de Gimeno MF. The involvement of nitric oxide in corpus luteum regression in the rat: feedback mechanism between prostaglandin F(2alpha) and nitric oxide. Mol Hum Reprod 1999; 5:1011–1016. PubMed
Noda Y, Ota K, Shirasawa T, Shimizu T. Copper/zinc superoxide dismutase insufficiency impairs progesterone secretion and fertility in female mice. Biol Reprod 2012; 86:1–8. PubMed
Gonzalez-Pacheco FR, Deudero JJ, Castellanos MC, Castilla MA, Alvarez-Arroyo MV, Yague S, Caramelo C. Mechanisms of endothelial response to oxidative aggression: protective role of autologous VEGF and induction of VEGFR2 by H2O2. Am J Physiol Heart Circ Physiol 2006; 291:H1395–H1401. PubMed
Wang K, Zheng J. Signaling regulation of fetoplacental angiogenesis. J Endocrinol 2012; 212:243–255. PubMed PMC
Brillo V, Chieregato L, Leanza L, Muccioli S, Costa R. Mitochondrial dynamics, ROS, and cell Signaling: a blended overview. Life (Basel) 2021; 11:332. PubMed PMC
Venditti P, Di Meo S. The role of reactive oxygen species in the life cycle of the mitochondrion. Int J Mol Sci 2020; 21:2173. PubMed PMC
Yoboue ED, Devin A. Reactive oxygen species-mediated control of mitochondrial biogenesis. Int J Cell Biol 2012; 2012:403870. PubMed PMC
Yan F, Zhao Q, Li Y, Zheng Z, Kong X, Shu C, Liu Y, Shi Y. The role of oxidative stress in ovarian aging: a review. J Ovarian Res 2022; 15:100. PubMed PMC
Gao X, Wang B, Huang Y, et al. Role of the Nrf2 Signaling pathway in ovarian aging: potential mechanism and protective strategies. Int J Mol Sci 2023; 24:13327. PubMed PMC
Goutami L, Jena SR, Swain A, Samanta L. Pathological role of reactive oxygen species on female reproduction. Adv Exp Med Biol 2022; 1391:201–220. PubMed
Shi L, Zhang J, Lai Z, Tian Y, Fang L, Wu M, Xiong J, Qin X, Luo A, Wang S. Long-term moderate oxidative stress decreased ovarian reproductive function by reducing follicle quality and progesterone production. PLoS One 2016; 11:e0162194. PubMed PMC
Yang L, Chen Y, Liu Y, Xing Y, Miao C, Zhao Y, Chang X, Zhang Q. The role of oxidative stress and natural antioxidants in ovarian aging. Front Pharmacol 2021; 11:617843. PubMed PMC
Yu C, Xiao JH. The Keap1-Nrf2 system: a mediator between oxidative stress and aging. Oxidative Med Cell Longev 2021; 2021:6635460. PubMed PMC
Liang J, Gao Y, Feng Z, Zhang B, Na Z, Li D. Reactive oxygen species and ovarian diseases: antioxidant strategies. Redox Biol 2023a; 62:102659. PubMed PMC
Lu J, Wang Z, Cao J, Chen Y, Dong Y. A novel and compact review on the role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2018a; 16:80. PubMed PMC
Supruniuk E, Baczewska M, Żebrowska E, Maciejczyk M, Lauko KK, Dajnowicz-Brzezik P, Milewska P, Knapp P, Zalewska A, Chabowski A. Redox biomarkers and matrix Remodeling molecules in ovarian cancer. Antioxidants 2024; 13:200. PubMed PMC
Zeber-Lubecka N, Ciebiera M, Hennig EE. Polycystic ovary syndrome and oxidative stress-from bench to bedside. Int J Mol Sci 2023; 24:14126. PubMed PMC
Juan CA, Perez de la Lastra JM, Plou FJ, Perez-Lebena E. The chemistry of reactive oxygen species (ROS) revisited: outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. Int J Mol Sci 2021; 22:4642. PubMed PMC
Surai PF, Kochish II, Fisinin VI, Juniper DT. Revisiting oxidative stress and the use of organic selenium in dairy cow nutrition. Animals 2019; 9:462. PubMed PMC
Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008; 4:278–286. PubMed
Upadhyay VR, Ramesh V, Dewry RK, Yadav DK, Ponraj P. Bimodal interplay of reactive oxygen and nitrogen species in physiology and pathophysiology of bovine sperm function. Theriogenology 2022; 187:82–94. PubMed
Adams L, Franco MC, Estevez AG. Reactive nitrogen species in cellular signaling. Exp Biol Med (Maywood) 2015; 240:711–717. PubMed PMC
Kapil V, Khambata RS, Jones DA, Rathod K, Primus C, Massimo G, Fukuto JM, Ahluwalia A. The noncanonical pathway for In vivo nitric oxide generation: the nitrate-nitrite-nitric oxide pathway. Pharmacol Rev 2020; 72:692–766. PubMed
Heinrich TA, da Silva RS, Miranda KM, Switzer CH, Wink DA, Fukuto JM. Biological nitric oxide signalling: chemistry and terminology. Br J Pharmacol 2013; 169:1417–1429. PubMed PMC
Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol 2020; 21:363–383. PubMed
Santos AL, Sinha S, Lindner AB. The good, the bad, and the ugly of ROS: new insights on aging and aging-related diseases from eukaryotic and prokaryotic model organisms. Oxidative Med Cell Longev 2018; 2018:1941285. PubMed PMC
Weidinger A, Kozlov AV. Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomol Ther 2015; 5:472–484. PubMed PMC
Dujíčková L, Olexiková L, Makarevich AV, Bartková AR, Němcová L, Chrenek P, Strejček F. Astaxanthin added during post-warm recovery mitigated oxidative stress in bovine vitrified oocytes and improved quality of resulting blastocysts. Antioxidants 2024; 13:556. PubMed PMC
Hejel P, Sáfár J, Bognár B, Kiss L, Jurkovich V, Brydl E, Könyves L. The impact of the oxidative status on the reproduction of cows and the calves' health - a review. Acta Vet Brno 2021; 90:3–13.
Jóźwik A, Krzyżewski J, Strzałkowska N, Poławska E, Bagnicka E, Wierzbicka A, Niemczuk K, Lipińska P, Horbańczuk JO. Relations between the oxidative status, mastitis, milk quality and disorders of reproductive functions in dairy cows - a review. Anim Sci Paper Rep 2012; 30:297–307.
Zhao XJ, Wang XY, Wang JH, Wang ZY, Wang L, Wang ZH. Oxidative stress and imbalance of mineral metabolism contribute to lameness in dairy cows. Biol Trace Elem Res 2015c; 164:43–49. PubMed
Abuelo A, Hernandez J, Benedito JL, Castillo C. The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation. J Anim Physiol Anim Nutr (Berl) 2015; 99:1003–1016. PubMed
Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 2014; 224:164–175. PubMed
Chainy GBN, Sahoo DK. Hormones and oxidative stress: an overview. Free Radic Res 2020; 54:1–26. PubMed
Cruz-Topete D, Dominic P, Stokes KY. Uncovering sex-specific mechanisms of action of testosterone and redox balance. Redox Biol 2020; 31:101490. PubMed PMC
Kochman J, Jakubczyk K, Bargiel P, Janda-Milczarek K. The influence of oxidative stress on thyroid diseases. Antioxidants 2021; 10:1442. PubMed PMC
Srinivasan V, Spence DW, Pandi-Perumal SR, Brown GM, Cardinali DP. Melatonin in mitochondrial dysfunction and related disorders. Int. J Alzheimers Dis 2011;2011:326320. PubMed PMC
Dutta S, Biswas A, Sengupta P, Nwagha U. Ghrelin and male reproduction. Asian Pac J Reprod 2019; 8:227–232.
Kurzawa R, Glabowski W, Baczkowski T, Wiszniewska B, Marchlewicz M. Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote 2004; 12:231–240. PubMed
Alvarez-Delgado C. The role of mitochondria and mitochondrial hormone receptors on the bioenergetic adaptations to lactation. Mol Cell Endocrinol 2022; 551:111661. PubMed
Baba SP, Bhatnagar A. Role of thiols in oxidative stress. Curr Opin Toxicol 2018; 7:133–139. PubMed PMC
Sies H. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol 2017; 11:613–619. PubMed PMC
Zandalinas SI, Mittler R. ROS-induced ROS release in plant and animal cells. Free Radic Biol Med 2018; 122:21–27. PubMed
Mailloux RJ. An update on mitochondrial reactive oxygen species production. Antioxidants (Basel) 2020; 9:472. PubMed PMC
Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 2011; 51:1289–1301. PubMed PMC
Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007; 87:245–313. PubMed
Vermot A, Petit-Hartlein I, Smith SME, Fieschi F. NADPH oxidases (NOX): an overview from discovery, molecular mechanisms to physiology and pathology. Antioxidants (Basel) 2021; 10:890. PubMed PMC
Li W, Young JF, Sun J. NADPH oxidase-generated reactive oxygen species in mature follicles are essential for drosophila ovulation. Proc Natl Acad Sci USA 2018; 115:7765–7770. PubMed PMC
Battelli MG, Polito L, Bortolotti M, Bolognesi A. Xanthine oxidoreductase-derived reactive species: physiological and pathological effects. Oxidative Med Cell Longev 2016; 2016:3527579. PubMed PMC
Isik H, Aynioglu O, Timur H, Sahbaz A, Harma M, Can M, Guven B, Alptekin H, Kokturk F. Is xanthine oxidase activity in polycystic ovary syndrome associated with inflammatory and cardiovascular risk factors? J Reprod Immunol 2016; 116:98–103. PubMed
Budani MC, Tiboni GM. Novel insights on the role of nitric oxide in the ovary: a review of the literature. Int J Environ Res Public Health 2021; 18:980. PubMed PMC
Tao Y, Fu Z, Zhang M, Xia G, Yang J, Xie H. Immunohistochemical localisation of inducible and endothelial nitric oxide synthase in porcine ovaries and effects of NO on antrum formation and oocyte meiotic maturation. Mol Cell Endocrinol 2004; 222:93–103. PubMed
Popov LD. Mitochondrial biogenesis: an update. J Cell Mol Med 2020; 24:4892–4899. PubMed PMC
Sahebnasagh A, Hashemi J, Khoshi A, Saghafi F, Avan R, Faramarzi F, Azimi S, Habtemariam S, Sureda A, Khayatkashani M, Safdari M, Rezai Ghaleno H, et al. Aromatic hydrocarbon receptors in mitochondrial biogenesis and function. Mitochondrion 2021; 61:85–101. PubMed
Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol 2003; 88:121–128. PubMed
Bishop DJ, Botella J, Genders AJ, Lee MJ, Saner NJ, Kuang J, Yan X, Granata C. High-intensity exercise and mitochondrial biogenesis: current controversies and future research directions. Physiology (Bethesda) 2019; 34:56–70. PubMed
Liang H, Ward WF. PGC-1alpha: a key regulator of energy metabolism. Adv Physiol Educ 2006; 30:145–151. PubMed
Vainshtein A, Tryon LD, Pauly M, Hood DA. Role of PGC-1alpha during acute exercise-induced autophagy and mitophagy in skeletal muscle. Am J Physiol Cell Physiol 2015; 308:C710–C719. PubMed PMC
Lee HC, Wei YH. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 2005; 37:822–834. PubMed
Kageyama M, Ito J, Shirasuna K, Kuwayama T, Iwata H. Mitochondrial reactive oxygen species regulate mitochondrial biogenesis in porcine embryos. J Reprod Dev 2021; 67:141–147. PubMed PMC
Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 2007; 47:143–183. PubMed
Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta 2016; 1863:2977–2992. PubMed
Killackey SA, Philpott DJ, Girardin SE. Mitophagy pathways in health and disease. J Cell Biol 2020; 219:e202004029. PubMed PMC
Ray B, Bhat A, Mahalakshmi AM, Tuladhar S, Bishir M, Mohan SK, Veeraraghavan VP, Chandra R, Essa MM, Chidambaram SB, Sakharkar MK. Mitochondrial and Organellar crosstalk in Parkinson's disease. ASN Neuro 2021; 13:1–10. PubMed PMC
Vincow ES, Merrihew G, Thomas RE, Shulman NJ, Beyer RP, MacCoss MJ, Pallanck LJ. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc Natl Acad Sci USA 2013; 110:6400–6405. PubMed PMC
Wang S, Chen Y, Li X, Zhang W, Liu Z, Wu M, Pan Q, Liu H. Emerging role of transcription factor EB in mitochondrial quality control. Biomed Pharmacother 2020; 128:110272. PubMed
Mansueto G, Armani A, Viscomi C, D'Orsi L, De Cegli R, Polishchuk EV, Lamperti C, Di Meo I, Romanello V, Marchet S, Saha PK, Zong H, et al. Transcription factor EB controls metabolic flexibility during exercise. Cell Metab 2017; 25:182–196. PubMed PMC
Olexiková L, Dujíčková L, Makarevich AV, Bezdíček J, Sekaninová J, Nesvadbová A, Chrene P. Glutathione during post-thaw recovery culture Can mitigate deleterious impact of Vitrification on bovine oocytes. Antioxidants 2023; 12:35. PubMed PMC
Richani D, Gilchrist RB. The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update 2018; 24:1–14. PubMed
Duffy DM, Ko C, Jo M, Brännström M, Curry TE. Ovulation: parallels with inflammatory processes. Endocr Rev 2019; 40:369–416. PubMed PMC
Espey LL, Stein VI, Dumitrescu J. Survey of antiinflammatory agents and related drugs as inhibitors of ovulation in the rabbit. Fertil Steril 1982; 38:238–247. PubMed
Gaytan M, Morales C, Bellido C, Sanchez-Criado JE, Gaytan F. Non-steroidal anti-inflammatory drugs (NSAIDs) and ovulation: lessons from morphology. Histol Histopathol 2006; 21:541–556. PubMed
Brännström M, Mayrhofer G, Robertson SA. Localisation of leukocyte subsets in the rat ovary during the periovulatory period. Biol Reprod 1993; 48:277–286. PubMed
Ho YS, Gargano M, Cao J, Bronson RT, Heimler I, Hutz RJ. Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J Biol Chem 1998; 273:7765–7769. PubMed
Miyazaki T, Sueoka K, Dharmarajan AM, Atlas SJ, Bulkley GB, Wallach EE. Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in-vitro perfused rabbit ovary. J Reprod Fertil 1991; 91:207–212. PubMed
Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N. Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci USA 2011; 108:1462–1467. PubMed PMC
Basini G, Tamanini C. Interrelationship between nitric oxide and prostaglandins in bovine granulosa cells. Prostaglandins Other Lipid Mediat 2001; 66:179–202. PubMed
Zerani M, Polisca A, Boiti C, Maranesi M. Current knowledge on the multifactorial regulation of corpora Lutea lifespan: the rabbit model. Animals (Basel) 2021; 11:296. PubMed PMC
Abdelnaby EA, El-Maaty AMA, Ragab RSA, Seida AA. Assessment of uterine vascular perfusion during the Estrous cycle of mares in connection to circulating leptin and nitric oxide concentrations. J Equine Vet Sci 2016; 39:25–32.
El-Sherry TM, Derar R, Bakry R. Changes in blood flow in ovine follicles and serum concentration of estradiol 17 beta (E2) and nitric oxide (NO) around the time of ovulation in Ossimi ewes. Anim Reprod Sci 2013; 138:188–193. PubMed
White RE. Estrogen and vascular function. Vasc Pharmacol 2002; 38:73–80. PubMed
Aréchiga-Flores C, Zimri CV, Hernández-Briano P, Flores-Flores G, Rochín-Berumen F, Ruiz-Fernández E. Review: function and regression of the corpus luteum during the estrous cycle. Abanico Veterinario 2019; 9:1–21.
Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll VA, Bicknell R. Suppression of luteal angiogenesis in the primate after neutralisation of vascular endothelial growth factor. Endocrinology 2000; 141:995–1000. PubMed
Kim YM, Kim SJ, Tatsunami R, Yamamura H, Fukai T, Ushio-Fukai M. ROS-induced ROS release orchestrated by Nox4, Nox2, and mitochondria in VEGF signaling and angiogenesis. Am J Physiol Cell Physiol 2017; 312:C749–C764. PubMed PMC
Chua CC, Hamdy RC, Chua BH. Upregulation of vascular endothelial growth factor by H2O2 in rat heart endothelial cells. Free Radic Biol Med 1998; 25:891–897. PubMed
Yoshioka S, Acosta TJ, Okuda K. Roles of cytokines and progesterone in the regulation of the nitric oxide generating system in bovine luteal endothelial cells. Mol Reprod Dev 2012; 79:689–696. PubMed
Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 2002; 277:29936–29944. PubMed
Tang W, Zhao G. Small molecules targeting HIF-1alpha pathway for cancer therapy in recent years. Bioorg Med Chem 2020; 28:115235. PubMed
Bonello S, Zahringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Gorlach A. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 2007; 27:755–761. PubMed
Brunelle JK, Bell EL, Quesada NM, Vercauteren K, Tiranti V, Zeviani M, Scarpulla RC, Chandel NS. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab 2005; 1:409–414. PubMed
Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U, Schumacker PT. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 2005; 1:401–408. PubMed
Parraguez VH, Urquieta B, Perez L, Castellaro G, De los Reyes M, Torres-Rovira L, Aguado-Martinez A, Astiz S, Gonzalez-Bulnes A. Fertility in a high-altitude environment is compromised by luteal dysfunction: the relative roles of hypoxia and oxidative stress. Reprod Biol Endocrinol 2013; 11:24. PubMed PMC
Farias JG, Bustos-Obregon E, Reyes JG. Increase in testicular temperature and vascularisation induced by hypobaric hypoxia in rats. J Androl 2005; 26:693–697. PubMed
Neuvians TP, Schams D, Berisha B, Pfaffl MV. Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2a-induced Luteolysis in bovine corpus luteum. Biol Reprod 2004; 70:473–480. PubMed
Okuda K, Uenoyama Y, Berisha B, Lange IG, Taniguchi H, Kobayashi S, Kobayashi S, Miyamoto A, Schams D. Estradiol-17b is produced in bovine corpus luteum. Biol Reprod 2001; 65:1634–1639. PubMed
Shirasuna K, Shimizu T, Hayashi KG, Nagai K, Matsui M, Miyamoto A. Positive association, in local release, of luteal oxytocin with endothelin 1 and prostaglandin F2alpha during spontaneous Luteolysis in the cow: a possible Intermediatory role for Luteolytic Cascade within the corpus luteum. Biol Reprod 2007; 76:965–970. PubMed
Przygrodzka E, Plewes MR, Davis JS. Luteinizing hormone regulation of inter-organelle communication and fate of the corpus luteum. Int J Mol Sci 2021; 22:9972. PubMed PMC
Al-Gubory KH, Garrel C, Faure P, Sugino N. Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress. Reprod Biomed Online 2012; 25:551–560. PubMed
Christenson LK, Devoto L. Cholesterol transport and steroidogenesis by the corpus luteum. Reprod Biol Endocrinol 2003; 1:90. PubMed PMC
Rekawiecki R, Nowik M, Kotwica J. Stimulatory effect of LH, PGE2 and progesterone on StAR protein, cytochrome P450 cholesterol side chain cleavage and 3beta hydroxysteroid dehydrogenase gene expression in bovine luteal cells. Prostaglandins Other Lipid Mediat 2005; 78:169–184. PubMed
Fridén BE, Runesson E, Hahlin M, Brännström M. Evidence for nitric oxide acting as a luteolytic factor in the human corpus luteum. Mol Hum Reprod 2000; 6:397–403. PubMed
Vega M, Johnson MC, Diaz HA, Urrutia LR, Troncoso JL, Devoto L. Regulation of human luteal steroidogenesis in vitro by nitric oxide. Endocrine 1998; 8:185–191. PubMed
Van Voorhis BJ, Dunn MS, Snyder GD, Weiner CP. Nitric oxide: an autocrine regulator of human granulosa-luteal cell steroidogenesis. Endocrinology 1994; 1994:1799–1806. PubMed
Masuda M, Kubota T, Aso T. Effects of nitric oxide on steroidogenesis in porcine granulosa cells during different stages of follicular development. Eur J Endocrinol 2001; 144:303–308. PubMed
Dave S, Farrance DP, Whitehead SA. Evidence that nitric oxide inhibits steroidogenesis in cultured rat granulosa cells. Clin Sci 1979; 92:277–284. PubMed
Jaroszewski JJ, Skarzynski DJ, Blair RM, Hansel W. Influence of nitric oxide on the secretory function of the bovine corpus luteum: dependence on cell composition and cell-to-cell communication. Exp Biol Med (Maywood) 2003a; 228:741–748. PubMed
Sugino N, Hirosawa-Takamori M, Zhong L, Telleria CM, Shiota K, Gibori G. Hormonal regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase messenger ribonucleic acid in the rat corpus luteum: induction by prolactin and placental lactogens. Biol Reprod 1998; 59:599–605. PubMed
Jablonka-Shariff A, Olson LM. Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro. Mol Reprod Dev 2000; 55:412–421. PubMed
Tiwari M, Chaube SK. Moderate increase of reactive oxygen species triggers meiotic resumption in rat follicular oocytes. J Obstet Gynaecol Res 2016; 42:536–546. PubMed
Yuan Y, Krisher R. 275 effect of reactive oxygen species during in vitro maturation on porcine oocyte nuclear maturation and developmental competence. Reprod Fertil Dev 2010; 23:235–236.
Curnow EC, Ryan JP, Saunders DM, Hayes ES. Developmental potential of bovine oocytes following IVM in the presence of glutathione ethyl ester. Reprod Fertil Dev 2010; 22:597–605. PubMed
Zhao XM, Min JT, Du WH, Hao HS, Liu Y, Qin T, Wang D, Zhu HB. Melatonin enhances the in vitro maturation and developmental potential of bovine oocytes denuded of the cumulus oophorus. Zygote 2015b; 23:525–536. PubMed
Almiñana C, Gil MA, Cuello C, Caballero I, Roca J, Vazquez JM, Gomez E, Martinez EA. In vitro maturation of porcine oocytes with retinoids improves embryonic development. Reprod Fertil Dev 2008; 20:483–489. PubMed
Gómez E, Royo LJ, Duque P, Carneiro G, Hidalgo C, Goyache F, Lorenzo PL, Alvarez I, Facal N, Diez C. 9-cis-retinoic acid during in vitro maturation improves development of the bovine oocyte and increases midkine but not IGF-I expression in cumulus-granulosa cells. Mol Reprod Dev 2003; 66:247–255. PubMed
Chaube SK, Prasad PV, Thakur SC, Shrivastav TG. Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro. Apoptosis 2005; 10:863–874. PubMed
Takami M, Preston SL, Toyloy VA, Behrman HR. Antioxidants reversibly inhibit the spontaneous resumption of meiosis. Am J Phys 1999; 276:E684–E688. PubMed
Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG, Chaube SK. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radic Res 2009; 43:287–294. PubMed
De Vos A, Van Steirteghem A. Zona hardening, zona drilling and assisted hatching: new achievements in assisted reproduction. Cells Tissues Organs 2000; 166:220–227. PubMed
Miao Y, Zhou C, Cui Z, Zhang M, ShiYang X, Lu Y, Xiong B. Postovulatory aging causes the deterioration of porcine oocytes via induction of oxidative stress. FASEB J 2018; 32:1328–1337. PubMed PMC
Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med 2008; 44:1295–1304. PubMed PMC
Zhang M, ShiYang X, Zhang Y, Miao Y, Chen Y, Cui Z, Xiong B. Coenzyme Q10 ameliorates the quality of postovulatory aged oocytes by suppressing DNA damage and apoptosis. Free Radic Biol Med 2019; 143:84–94. PubMed
Preutthipan S, Chen SH, Tilly JL, Kugu K, Lareu RR, Dharmarajan AM. Inhibition of nitric oxide synthesis potentiates apoptosis in the rabbit corpus luteum. Reprod Biomed Online 2004; 9:264–270. PubMed
Miyamoto A, Shirasuna K. Luteolysis in the cow: a novel concept of vasoactive molecules. Anim Reprod 2009; 6:47–59.
Korzekwa A, Woclawek-Potocka I, Okuda K, Acosta TJ, Skarzynski DJ. Nitric oxide in bovine corpus luteum: possible mechanisms of action in luteolysis. Anim Sci J 2007; 78:233–242.
Jaroszewski JJ, Bogacki M, Skarzynski DJ. Progesterone production in bovine luteal cells treated with drugs that modulate nitric oxide production. Reproduction 2003; 125:389–395. PubMed
Skarzynski DJ, Okuda K. Different actions of noradrenaline and nitric oxide on the output of prostaglandins and progesterone in cultured bovine luteal cells. Prostaglandins Other Lipid Mediat 2000; 2008:35–47. PubMed
Skarzynski DJ, Jaroszewski JJ, Bah MM, Deptula KM, Barszczewska B, Gawronska B, Hansel W. Administration of a nitric oxide synthase inhibitor counteracts prostaglandin F2-induced luteolysis in cattle. Biol Reprod 2003; 68:1674–1681. PubMed
Weems YS, Lennon E, Uchima T, Raney A, Goto K, Ong A, Zaleski H, Weems CW. Mechanism whereby nitric oxide (NO) infused chronically intrauterine in ewes is antiluteolytic rather than being luteolytic. Prostaglandins Other Lipid Mediat 2008; 85:33–41. PubMed
Liszewska E, Rekawiecki R, Kotwica J. Effect of progesterone on the expression of bax and bcl-2 and on caspase activity in bovine luteal cells. Prostag Lipid Mediat 2005; 78:67–81. PubMed
Vallcaneras S, Morales L, Delsouc MB, Ramirez D, Filippa V, Fernandez M, Telleria CM, Casais M. Interplay between nitric oxide and gonadotrophin-releasing hormone in the neuromodulation of the corpus luteum during late pregnancy in the rat. Reprod Biol Endocrinol 2022; 20:19. PubMed PMC
Lashari MH, Tasawar Z. The effect of PGF2α on persistent corpus luteum in Sahiwal cows. Int J Livest Prod 2012; 3:1–5.
Mogheiseh A, Ahmadi MR, Nazifi S, Mirzaei A, Fallah E. Destination of corpus luteum in postpartum clinical endometritis cows and factors affecting self-recovery. Vet Anim Sci 2020; 9:100067. PubMed PMC
Vu HV, Lee S, Acosta TJ, Yoshioka S, Abe H, Okuda K. Roles of prostaglandin F2alpha and hydrogen peroxide in the regulation of copper/zinc superoxide dismutase in bovine corpus luteum and luteal endothelial cells. Reprod Biol Endocrinol 2012; 10:87. PubMed PMC
Rapoport R, Sklan D, Wolfenson D, Shaham-Albalancy A, Hanukoglu I. Antioxidant capacity is correlated with steroidogenic status of the corpus luteum during the bovine estrous cycle. Biochim Biophys Acta 1998; 1380:133–140. PubMed
Perkins A, Nelson KJ, Parsonage D, Poole LB, Karplus PA. Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem Sci 2015; 40:435–445. PubMed PMC
Rhee SG, Kil IS. Multiple functions and regulation of mammalian Peroxiredoxins. Annu Rev Biochem 2017; 86:749–775. PubMed
Park HJ, Lee DG, Seong JB, Lee HS, Kwon OS, Kang BS, Park JW, Lee SR, Lee DS. Peroxiredoxin I maintains luteal function by regulating unfolded protein response. Reprod Biol Endocrinol 2018; 16:79. PubMed PMC
Park SJ, Kim JH, Kim TS, Lee SR, Park JW, Lee S, Kim JM, Lee DS. Peroxiredoxin 2 regulates PGF2alpha-induced corpus luteum regression in mice by inhibiting ROS-dependent JNK activation. Free Radic Biol Med 2017; 108:44–55. PubMed
Qian Y, Shao L, Yuan C, Jiang CY, Liu J, Gao C, Gao L, Cui YG, Jiang SW, Liu JY, Meng Y. Implication of differential Peroxiredoxin 4 expression with age in ovaries of mouse and human for ovarian aging. Curr Mol Med 2016; 16:243–251. PubMed
Rueda BR, Tilly KI, Hansen TR, Hoyer PB, Tilly JL. Expression of superoxide dismutase, catalase and glutathione peroxidase in the bovine corpus luteum: evidence supporting a role for oxidative stress in luteolysis. Endocrine 1995; 3:227–232. PubMed
Sugino N. Reactive oxygen species in ovarian physiology. Reprod Med Biol 2005; 4:31–44. PubMed PMC
Sugino N. Roles of reactive oxygen species in the corpus luteum. Anim Sci J 2006; 77:556–565.
Sugino N, Takiguchi S, Kashida S, Karube A, Nakamura Y, Kato H. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Mol Hum Reprod 2000; 6:19–25. PubMed
Riley JC, Behrman HR. In vivo generation of hydrogen peroxide in the rat corpus luteum during luteolysis. Endocrinology 1991; 128:1749–1753. PubMed
Sugimoto Y, Yamasaki A, Segi E, Tsuboi K, Aze Y, Nishimura T, Oida H, Yoshida N, Tanaka T, Katsuyama M, Hasumoto K, Murata T, et al. Failure of parturition in mice lacking the prostaglandin F receptor. Science 1997; 277:681–683. PubMed
Wiltbank MC, Ottobre JS. Regulation of intraluteal production of prostaglandins. Reprod Biol Endocrinol 2003; 1:91. PubMed PMC
Taniguchi K, Matsuoka A, Kizuka F, Lee L, Tamura I, Maekawa R, Asada H, Taketani T, Tamura H, Sugino N. Prostaglandin F2alpha (PGF2alpha) stimulates PTGS2 expression and PGF2alpha synthesis through NFKB activation via reactive oxygen species in the corpus luteum of pseudopregnant rats. Reproduction 2010; 140:885–892. PubMed
Benyo DF, Pate JL. Tumor necrosis factor-alpha alters bovine luteal cell synthetic capacity and viability. Endocrinology 1992; 130:854–860. PubMed
Bagnjuk K, Stockl JB, Frohlich T, Arnold GJ, Behr R, Berg U, Berg D, Kunz L, Bishop C, Xu J, Mayerhofer A. Necroptosis in primate luteolysis: a role for ceramide. Cell Death Dis 2019; 5:67. PubMed PMC
Motta AB, Estevez A, Franchi A, Perez-Martinez S, Farina M, Ribeiro ML, Lasserre A, Gimeno MF. Regulation of lipid peroxidation by nitric oxide and PGF2alpha during luteal regression in rats. Reproduction 2001; 121:631–637. PubMed
Motta AB, Franchi AM, Gimeno MF. Role of nitric oxide on uterine and ovarian prostaglandin synthesis during luteolysis in the rat. Prostaglandins Leukot Essent Fatty Acids 1997; 56:265–269. PubMed
Motta AB, Gimeno MA. Nitric oxide participates in the corpus luteum regression in ovaries isolated from pseudopregnant rats. Can J Physiol Pharmacol 1997; 75:1335–1339. PubMed
Jaroszewski JJ, Skarzynski DJ, Hansel W. Nitric oxide as a local mediator of prostaglandin F2alpha-induced regression in bovine corpus luteum: an in vivo study. Exp Biol Med (Maywood) 2003b; 228:1057–1062. PubMed
Foyouzi N, Cai Z, Sugimoto Y, Stocco C. Changes in the expression of steroidogenic and antioxidant genes in the mouse corpus luteum during luteolysis. Biol Reprod 2005; 72:1134–1141. PubMed
Hojo T, Siemieniuch MJ, Lukasik K, Piotrowska-Tomala KK, Jonczyk AW, Okuda K, Skarzynski DJ. Programmed necrosis - a new mechanism of steroidogenic luteal cell death and elimination during luteolysis in cows. Sci Rep 2016; 6:38211. PubMed PMC
Nishimura R, Sakumoto R, Tatsukawa Y, Acosta TJ, Okuda K. Oxygen concentration is an important factor for modulating progesterone synthesis in bovine corpus luteum. Endocrinology 2006; 147:4273–4280. PubMed
Boiti C, Guelfi G, Zampini D, Brecchia G, Gobbetti A, Zerani M. Regulation of nitric oxide synthase isoforms and role of nitric oxide during prostaglandin F2alpha-induced luteolysis in rabbits. Reproduction 2003; 125:807–816. PubMed
Vega M, Urrutia L, Iniguez G, Gabler F, Devoto L, Johnson MC. Nitric oxide induces apoptosis in the human corpus luteum in vitro. Mol Hum Reprod 2000; 6:681–687. PubMed
Shirasuna K, Watanabe S, Asahi T, Wijayagunawardane MP, Sasahara K, Jiang C, Matsui M, Sasaki M, Shimizu T, Davis JS, Miyamoto A. Prostaglandin F2alpha increases endothelial nitric oxide synthase in the periphery of the bovine corpus luteum: the possible regulation of blood flow at an early stage of luteolysis. Reproduction 2008; 135:527–539. PubMed
Shirasuna K. Nitric oxide and luteal blood flow in the luteolytic cascade in the cow. J Reprod Dev 2010; 56:9–14. PubMed
Weems YS, Lennon E, Uchima T, Raney A, Goto K, Ong A, Zaleski H, Weems CW. Is nitric oxide luteolytic or antiluteolytic? Prostaglandins Other Lipid Mediat 2005; 78:129–138. PubMed
Best MP, Frimberger AE. Ovarian carcinomatosis in a dog managed with surgery and intraperitoneal, systemic, and intrapleural chemotherapy utilizing indwelling pleural access ports. Can Vet J 2017; 58:493–497. PubMed PMC
Vanderhyden BC, Shaw TJ, Ethier JF. Animal models of ovarian cancer. Reprod Biol Endocrinol 2003; 1:67. PubMed PMC
Hense JD, Isola JVV, Garcia DN, et al. The role of cellular senescence in ovarian aging. Aging 2024; 10:35. PubMed PMC
Wang X, Wang L, Xiang W. Mechanisms of ovarian aging in women: a review. J Ovarian Res 2023; 16:67. PubMed PMC
Zhu Z, Xu W, Liu L. Ovarian aging: mechanisms and intervention strategies. Medical Rev 2021; 2:590–610. PubMed PMC
Sasaki H, Hamatani T, Kamijo S, Iwai M, Kobanawa M, Ogawa S, Miyado K, Tanaka M. Impact of oxidative stress on age-associated decline in oocyte developmental competence. Front Endocrinol 2019; 2019:811. PubMed PMC
Rizzo A, Roscino MT, Binetti F, Sciorsci RL. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim 2012; 47:344–352. PubMed
Kaspar JW, Niture SK, Jaiswal AK. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009; 47:1304–1309. PubMed PMC
Bellezza I, Giambanco I, Minelli A, Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta, Mol Cell Res 2018; 1865:721–733. PubMed
Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, Lamas S. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol 2015; 6:183–197. PubMed PMC
Ma R, Liang W, Sun Q, Qiu X, Lin Y, Ge X, Jueraitetibaike K, Xie M, Zhou J, Huang X, Wang Q, Che L. Sirt1/Nrf2 pathway is involved in oocyte aging by regulating cyclin B1. Aging 2018; 2018:2991–3004. PubMed PMC
Sze SCW, Zhang L, Zhang S, Lin K, Ng B, Ng ML, Lee KF, Lam JKW, Zhang Z, Yung KKL. Aberrant transferrin and ferritin upregulation elicits iron accumulation and oxidative Inflammaging causing Ferroptosis and undermines Estradiol biosynthesis in aging rat ovaries by upregulating NF-Κb-activated inducible nitric oxide synthase: first demonstration of an intricate mechanism. Int J Mol Sci 2022; 23:12689. PubMed PMC
Sadeghi HM, Adeli I, Calina D, Docea AO, Mousavi T, Daniali M, Nikfar S, Tsatsakis A, Abdollahi M. Polycystic ovary syndrome: a comprehensive review of pathogenesis, management, and drug repurposing. Int J Mol Sci 2022; 23:583. PubMed PMC
Stener-Victorin E, Teede H, Norman RJ, Legro R, Goodarzi MO, Dokras A, Laven J, Hoeger K, Piltonen TT. Polycystic ovary syndrome. Nat Rev Dis Primers 2024; 10:27. PubMed
Li W, Liu C, Yang Q, Zhou Y, Liu M, Shan H. Oxidative stress and antioxidant imbalance in ovulation disorder in patients with polycystic ovary syndrome. Front Nutr 2022; 9:1018674. PubMed PMC
Zuo T, Zhu M, Xu W. Roles of oxidative stress in polycystic ovary syndrome and cancers. Oxidative Med Cell Longev 2016;2016:8589318. PubMed PMC
Rudnicka E, Duszewska AM, Kucharski M, Tyczyński P, Smolarczyk R. Oxidative stress and reproductive function: oxidative stress in polycystic ovary syndrome. Reproduction 2022; 164:F145–F154. PubMed
Awonuga AO, Camp OG, Abu-Soud HM. A review of nitric oxide and oxidative stress in typical ovulatory women and in the pathogenesis of ovulatory dysfunction in PCOS. Reprod Biol Endocrinol 2023; 21:111. PubMed PMC
Nácul AP, Andrade CD, Schwarz P, de Bittencourt PI, Jr, & Spritzer PM. Nitric oxide and fibrinogen in polycystic ovary syndrome: associations with insulin resistance and obesity. Eur J Obstet Gynecol Reprod Biol 2007; 133:191–196. PubMed
Krishna MB, Joseph A, Thomas PL, Dsilva B, Pillai SM, Laloraya M. Impaired arginine metabolism coupled to a defective redox conduit contributes to low plasma nitric oxide in polycystic ovary syndrome. Cell Physiol Biochem 2017; 43:1880–1892. PubMed
Meng C. Nitric oxide (NO) levels in patients with polycystic ovary syndrome (PCOS): a meta-analysis. J Int Med Res 2019; 47:4083–4094. PubMed PMC
Kodama H, Fukuda J, Karube H, Matsui T, Shimizu Y, Tanaka T. High incidence of embryo transfer cancellations in patients with polycystic ovarian syndrome. Hum Reprod 1995; 10:1962–1967. PubMed
Hyderali BN, Mala K. Oxidative stress and cardiovascular complications in polycystic ovarian syndrome. Eur J Obstet Gynecol Reprod Biol 2015; 191:15–22. PubMed
Bódis J, Várnagy A, Sulyok E, Kovács GL, Martens-Lobenhoffer J, Bode-Böger SM. Negative association of L-arginine methylation products with oocyte numbers. Hum Reprod 2010; 25:3095–3100. PubMed
Li T, Zhang T, Wang H, Zhang Q, Gao H, Liu R, Yin C. The ADMA-DDAH1 axis in ovarian apoptosis of polycystic ovary syndrome. J Steroid Biochem Mol Biol 2023; 225:106180. PubMed
Caldwell RW, Rodriguez PC, Toque HA, Narayanan SP, Caldwell RB. Arginase: a multifaceted enzyme important in health and disease. Physiol Rev 2018; 98:641–665. PubMed PMC
Kyselova A, Hinrichsmeyer H, Zukunft S, Mann AW, Dornauf I, Fleming I, Randriamboavonjy V. Association between arginase-containing platelet-derived microparticles and altered plasma arginine metabolism in polycystic ovary syndrome. Metabolism 2019; 90:16–19. PubMed
Stewart C, Ralyea C, Lockwood S. Ovarian cancer: an integrated review. Semin Oncol Nurs 2019; 35:151–156. PubMed
Meshkovska Y, Abramov A, Mahira S, Thatikonda S. Understanding the impact of oxidative stress on ovarian cancer: advances in diagnosis and treatment. Future Pharmacol 2024; 4:651–675.
Santosh SW, Freddy AJ, Winkins D. Oxidative Stress in the Pathogenesis of Ovarian Cancer. In: Chakraborti S (ed.), Handbook of Oxidative Stress in Cancer: Therapeutic Aspects. Singapore: Springer; 2022.
Chan DW, Liu VW, Tsao GS, Yao KM, Furukawa T, Chan KK, Ngan HY. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 2008; 29:1742–1750. PubMed
Liu LZ, Hu XW, Xia C, He J, Zhou Q, Shi X, Fang J, Jiang BH. Reactive oxygen species regulate epidermal growth factor-induced vascular endothelial growth factor and hypoxia-inducible factor-1α expression through activation of AKT and P70S6K1 in human ovarian cancer cells. Free Radic Biol Med 2006; 41:1521–1533. PubMed
Xia C, Meng Q, Liu LZ, Rojanasakul Y, Wang XR, Jiang BH. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res 2007; 67:10823–10830. PubMed
Stieg DC, Wang Y, Liu L-Z, Jiang B-H. ROS and miRNA dysregulation in ovarian cancer development, angiogenesis and therapeutic resistance. Int J Mol Sci 2022; 23:6702. PubMed PMC
Xiong X, Liao X, Qiu S, Xu H, Zhang S, Wang S, Ai J, Yang L. CXCL8 in tumor biology and its implications for clinical translation. Front Mol Biosci 2022; 9:723846. PubMed PMC
Qiu J, Xu Q, Panah T, Morshed AKMH, Wang X, Zhou F, Liu W, Wang J, Zhang Y, Liu B, Jiang BH. Reactive oxygen species mediate ovarian cancer development, platinum resistance, and angiogenesis via CXCL8 and GSK-3β/p70S6K1 axis. Genes Dis 2024;12:101378. PubMed PMC
Kielbik M, Szulc-Kielbik I, Klink M. The potential role of iNOS in ovarian cancer progression and chemoresistance. Int J Mol Sci 2019; 20:1751. PubMed PMC
Burke AJ, Garrido P, Johnson C, Sullivan FJ, Glynn SA. Inflammation and Nitrosative stress effects in ovarian and prostate pathology and carcinogenesis. Antioxid Redox Signal 2017; 26:1078–1090. PubMed
Chen L, Tang Q, Zhang K, Huang Q, Ding Y, Jin B, Liu S, Hwa K, Chou CJ, Zhang Y, Thyparambil S, Liao W, et al. Altered expression of the L-arginine/nitric oxide pathway in ovarian cancer: metabolic biomarkers and biological implications. BMC Cancer 2023; 23:844. PubMed PMC
El-Sehemy A, Postovit LM, Fu Y. Nitric oxide signaling in human ovarian cancer: a potential therapeutic target. Nitric Oxide 2016; 54:30–37. PubMed
Stevens EV, Carpenter AW, Shin JH, Liu J, Der CJ, Schoenfisch MH. Nitric oxide-releasing silica nanoparticle inhibition of ovarian cancer cell growth. Mol Pharm 2010; 7:775–785. PubMed PMC